Cent. Eur. J. Biol. • 9(1) • 2014 • 11-18 DOI: 10.2478/s11535-013-0120-6 Central European Journal of Biology Enemy at the gates: introduction potential of non-indigenous freshwater crayfish in Greece via the aquarium trade Research Article Irene Papavlasopoulou1, Costas Perdikaris2,*, Leonidas Vardakas3, Ioannis Paschos4 1Department of Veterinary Medicine, University of Thessaly and Department of Aquaculture & Fisheries, Technological Educational Institute of Epirus, 43100 Karditsa, Greece 2Department of Fisheries, Regional Unit of Thesprotia, Region of Epirus, 46100 Igoumenitsa, Greece 3Institute of Inland Waters, Hellenic Centre for Marine Research, 19013 Anavissos, Greece 4Department of Aquaculture & Fisheries, Technological Educational Institute of Epirus, 46100 Igoumenitsa, Greece Received 11 May 2012; Accepted 23 October 2012 Abstract: Indigenousfreshwater crayfish species (ICS) are important biodiversity components and desirable fishery targets. However,ICS populationsareincreasinglythreatenedbyvariousanthropogenicstressors.Moreover,establishedpopulationsofnon-indigenous freshwatercrayfishspecies(NICS)andnew‘waves’ofNICSintroductionsexertsignificantpressureonICSpopulationsatapan- Europeanlevel.Theseeffectsincludedirectcompetitionforspaceandresourcesaswellascrayfish‘plague’transmissionfrom introduced North American species. Given low public knowledge of this problematic, considerable risk of future introductions exist as a result of conventional and internet-based aquarium trade, which often lead to deliberate and/or accidental releases of NICS into the wild. In 2011, we conducted a survey of freshwater crayfish species in eleven large-size pet shops located in three major cities and in three large internet-based aquarium companies in Greece. Overall, eight species belonging to three genera (Procambarus, Cherax and Cambarellus) were recorded, originating from the USA, Australia, New Guinea and Mexico. The invasion potential of the three most popular species was assessed using the Freshwater Invertebrate Invasiveness Scoring Kit (FI-ISK). Two species were determined to constitute a ‘very high risk’ of invasion. As such, regulatory measures need to be implemented to monitor the ornamental trade of NICS in Greece and a national framework developed for protecting ICS. Keywords: Aquarium trade • Biodiversity • FI-ISK • Non-indigenous freshwater crayfish ©VersitaSp.zo.o. 1. Introduction eutrophication and overexploitation [1]. Furthermore, increasing information on NICS introductions into European Several populations of indigenous freshwater crayfish freshwaters [2] indicates a serious risk of extinction for species (ICS) in Europe are at risk of becoming local populations in the near future through both direct endangered or extinct as a result of various anthropogenic (e.g. predation and crayfish ‘plague’) and indirect effects stressors such as the crayfish ‘plague’ disease, other (e.g. grazing of aquatic macrophytes, alteration of diseases, competition with invasive non-indigenous biomass and species richness of macroinvertebrates, crayfish species (NICS), translocations of both ICS and bank erosion and substrate disturbance) [3]. The latter NICS, loss of genetic diversity, pollution, water abstraction could exert dramatic changes to the biodiversity of aquatic for irrigation and direct human use, habitat destruction, communities and the integrity of ecosystems in Europe. * E-mail: [email protected] 11 Enemy at the gates: introduction potential of non-indigenous freshwater crayfish in Greece via the aquarium trade Recent efforts to review and record historical and (FI-ISK) tool developed by the Centre for Environment current occurrences of ICS in Greece [4-6] showed Fisheries and Aquaculture Science (CEFAS) that crayfish populations are present in at least 34 (http://cefas.defra.gov.uk/our-science/ecosystems-and- hydrographic systems (natural and man-made lakes, biodiversity/non-native-species/decision-support-tools. rivers and small streams). However, the distribution aspx) to assess the invasion potential of the three most of crayfish is much more restricted nowadays than popular aquarium species (Procambarus clarkii, Cherax in previous decades, and many populations of ICS destructor and Cherax quadricarinatus). The same tool are isolated and confined to headwaters and lentic was also applied to ICS and NICS in Greek freshwaters environments that remain pristine [4]. Although there systems for comparison purposes. is only one established population of invasive NICS (i.e. signal crayfish Pacifastacus leniusculus (Dana, 1852)), ICS (noble crayfish Astacus astacus (L.), 3. Results narrowclawed crayfish Astacus leptodactylus Eschscholtz 1823, stone crayfish Austropotamobius Overall, we recorded eight species of NICS belonging torrentium (Schrank, 1803)) and their habitats are to three genera (Table 1). Available data for four species confronted to serious threats due to human-mediated (Procambarus clarkii, Cherax quardicarinatus, Cherax stressors. These threats are expected to be exacerbated peknyi and Cambarellus patzcuarensis) suggested that by globalization leading to increased trade and they were imported from Singapore. C. quardicarinatus e-commerce of NICS, unrestricted movement/travelling may also have been imported from an alternative of NICS, intense economic activity, demographic location in Italy. The species most advertised for sale in pressures [7,8] and climate change, which generally the e-commerce were P. clarkii and C. quadricarinatus. favour NICS with less strict ecological preferences and The FI-ISK revealed that invasion potential was increased adaptive ability compared to ICS [3]. Recently, particularly high for P. clarkii and C. destructor. The astacologists have determined that the aquarium trade analysis rejected these species for introduction in is as one of the most important and plausible sources of the aquarium trade based on a 16 points threshold. NICS introductions in Europe and worldwide. However C. quadricarinatus had moderate score, requiring data on the Hellenic aquarium trade of NICS is lacking. further assessment for introduction. The FI-ISK scores So far, aquatic ecologists have focused on studying are presented in Figure 1 against: (a) the scores for the and managing ecosystems already invaded and three ICS and the only NICS established in Greece; and degraded by non-indigenous species. Precautionary (b) the scores generated by Tricarico et al. [9] for the measures are urgently needed for mitigating further same species in Italy. Accurate scoring for C. peknyi, introductions of non-indigenous species, one of the P. alleni, C. shufeldtii, C. montezuma and most important threats to biodiversity worldwide. Here, C. patzcuarensis was not possible due to the limited our objective was to record the presence of ornamental bibliographic data on their biology and invasion ecology. NICS in the Greek aquarium trade market and assess their invasion potential into the wild. 4. Discussion 2. Experimental Procedures European ICS populations have suffered from serious declines during the last century, mainly due to the spread We recorded the presence of NICS in eleven large- of the crayfish ‘plague’ diseasevia introduced American size aquarium stores in Greece’s two largest cities species. All crayfish of Northern and Central American (Athens and Thessaloniki) and one large provincial origin, such as species from the genera Pacifastacus, city (Ioannina) between January and December 2011. Procambarus, Cambarellus and Orconectes are We also conducted an online-based research of three suspected vectors of crayfish ‘plague’. Freshwater major internet-based companies with stores in the crayfish are particularly good invaders compared to Greek pet market simultaneously. Data on the number other groups of aquatic organisms. Currently, ten of sales per store were not available. However, we NICS are established in the European freshwaters anecdotally recorded that nine specimens of the most with establishment success record approaching 100%, ornamental and large-size C. quardicarinatus were compared to the number of introduced species to the wild sold during 2011 in one store in the city of Ioannina [10]. Although NICS are still absent from neighbouring with a population of 100,000 inhabitants. We used the countries to Greece (i.e., Albania, the former Yugoslav Freshwater Invertebrate Invasiveness Scoring Kit, v1.19 Republic of Macedonia, Bulgaria, and Turkey) [2,5], 12 I. Papavlasopoulou I. Papavlasopoulou Common Native Documented/ Species Authority Abbreviation Basic biological features Habitat preferences Source name origin possible impacts Very highly invasive ability, Reproduction >10°C, temperature carrier of the ‘plague’, tolerant ≤35ºC (best growth: 22-30ºC), competition with ICS for space Lentic including saline et al. r-selected, breeding capacity over 600 and resources, structural waters (swamps, eggs, rapid growth, life span: changes in food webs, marshes seasonally Procambarus Red swamp S.E United 4 years, max length: 15 cm TL, tolerant predation, bioaccumulation, Girard, 1852 PCC flooded wetlands, [3,20,25,26] clarkii crayfish States of brackish water (12 psu) and adverse elimination/reduction of slow flowing water, environmental conditions (e.g. lower abundance and richness of reservoirs, irrigation dissolved oxygen lethal limit of indigenous species, damages systems, rice fields). 0.4 mg/L), burrowing ability, to agricultural crops, ditches omnivorous-polytrophic. and river banks, increased